The Chicago native began his coaching career in 1978 with back to back year long stints as an assistant coach at Oak Lawn Community High School and De La Salle Institute. Callahan started his college coaching career shortly after in 1980 as a graduate assistant at University of Illinois before being promoted to full-time assistant in 1981, coaching tight ends, offensive line, quarterbacks and special teams through 1986.

Callahan served a two-year stint, 1987–1988, as offensive line coach at Northern Arizona University and one year as offensive coordinator of Southern Illinois in 1989. From 1990–1994, Callahan was offensive line coach at the University of Wisconsin–Madison. He has been praised by former Wisconsin coach Barry Alvarez as being one of the primary reasons why the Badgers were able to turn their program around and eventually win three Rose Bowls in the 1990s. Alvarez cited Callahan specifically for his strong recruiting abilities.

At Southern Illinois in 1989,[1] he led an offense that ran for 1,245 yards and threw for 2,569 yards with 19 TD. As of 2011, the 238 completions and 432 pass attempts were 2nd most in school history in both categories.

At Wisconsin[2] after a 1-10 season in 1990, he helped pave the way for Terrell Fletcher to run for 446 yards in 1991. In 1992, that number jumped to 492 and Brent Moss ran for 739 yards and 9 TD. By 1993, Wisconsin's offensive line paved the way for Moss' 1,637 yards and 16 TD. Fletcher also ran for 996 and 9 TD. QB Darrell Bevell was able to throw for 19 TD. In 1994, Bevell would throw 17 TD and Fletcher would run for 1,476 yards and 12 TD while Moss ran for 833 yards and 8 TD. Some of the OL that Callahan coached during this period included: Joe Panos, Joe Rudolph, Steve Stark, Mike Verstagen, and Cory Raymer.

Callahan started his NFL career as the offensive line coach for the Philadelphia Eagles from 1995 to 1997. He then spent four seasons as the Oakland Raiders offensive coordinator before being named the franchise's 13th head coach prior to the 2002 season. Callahan was the head coach of the Oakland Raiders of the NFL during the 2002 and 2003 seasons.

In his first season as a head coach, led the Raiders to a third consecutive AFC West title and the franchise's first Super Bowl since returning to Oakland, making him just the fourth rookie head coach in NFL history to do so. The Raiders suffered a lopsided defeat in Super Bowl XXXVII losing 48–21 to the Tampa Bay Buccaneers coached by his former boss Jon Gruden. This was largely because Callahan kept Gruden's old playbook more or less intact, and the Bucs had received so much information about the Raiders' offensive scheme from Gruden that they knew exactly what plays were coming.[3][4] It did not help that the Raiders were without starting center Barret Robbins, the leader of their offensive line. Robbins went into a manic episode after not taking his medication, and spent most of the day before the game in Tijuana believing the Raiders had already won. When he finally resurfaced, he was so incoherent that Callahan had no choice but to leave him off the roster.

Callahan is the third Raiders head coach to win an AFC West title and lead his team into the conference championship game in his first full season. Only Art Shell (1990) and John Madden (1969) had accomplished this feat.

Under Callahan's guidance, the Raiders led the NFL in passing for the first time in team history and led the league in total offense for just the second time in team history.

During his tenure as not only head coach but also offensive coordinator for the Raiders, the Raider offense led the league in rushing in 2000 and led the league in passing in 2002. In 2002, the Raiders became the first team to win games in the same season while rushing at least 60 times (against Kansas City in a 24–0 win) and passing at least 60 times (against Pittsburgh in a 30–17 win). The Raider offense also set many franchise records during this period, including fewest sacks allowed (28) in 2000, a mark that was broken the following year (27).

Despite the success of his 2002 team, the 2003 Raiders had a losing record. After his team got off to a 2–5 start, many of his players, in particular Charles Woodson, publicly criticized the coach, even suggesting that Callahan was deliberately trying to sabotage the season. According to Woodson, the Raider locker room was almost in a state of mutiny against Callahan, a claim corroborated by veteran receiver Tim Brown and others. Callahan, his supporters claim, had recognized that the team was aging and needed younger talent. To get it, he would have to cut existing salaries, an assertion that did not sit well with many of the team's veterans. It did not help that quarterback Rich Gannon was sidelined with injuries for much of the season. On Nov 30, after a 22–8 loss to the Denver Broncos, Callahan said the Raiders must have been "the dumbest team in America in terms of playing the game." After a lackluster 4–12 season, Callahan was fired by Raiders owner Al Davis. Even though the Raiders had gone all the way to the Super Bowl a year earlier, Davis was not known for being patient with his coaches. Callahan was the last Raiders coach to post a winning season until 2016.

In January 2013, Callahan was publicly accused of sabotaging Super Bowl XXXVII by several former players.[5] According to comments by Tim Brown and others, the Raiders struggled on offense during the Super bowl because of Callahan changing the game plan from a heavy run attack to a heavy passing one on the Friday before the game. Although some claim this was due to the Barrett Robbins incident, Brown offered no proof for the sabotage claim, but said: "this is the problem we have, because of Callahan's relationship with Gruden, because of his disdain for the Raider organization; that's what makes people get to that conclusion."[5]Rich Gannon defended Callahan, but did suggest that Oakland may have been disadvantaged by Callahan's failure to change the terminology for play calls at the line of scrimmage. According to Gannon, the same play names had been used during Gruden's tenure as Raiders coach, and Gruden had taught his Buccaneers defensive players these play names.[6]

Jerry Rice, an NFL Hall of Famer who was a wide receiver for the Raiders at that time, was quoted as saying, "I was very surprised that he waited till the last second and I think a lot of the players they were surprised also so in a way maybe because he didn't like the Raiders he decided 'Hey look maybe we should sabotage just a little bit and let Jon Gruden go out and win this one.'"[7]

Callahan has denied the allegations, stating that, "While I fully understand a competitive professional football player's disappointment when a game's outcome doesn't go his team's way, I am shocked, saddened and outraged by Tim Brown's allegations and Jerry Rice's support of those allegations made through various media outlets over the last 24 hours. To leave no doubt, I categorically and unequivocally deny the sum and substance of their allegations." Callahan further referred to the claim as "ludicrous and defamatory."[7]

Brown backtracked from his comments a day later, denying having said that Callahan sabotaged the game.[8]

Soon after being fired by the Raiders, Callahan was hired at Nebraska. This would mark the first time in over four decades (since the hiring of Bob Devaney in 1962) that the Cornhuskers would be led by a head coach with no direct ties to the university either as a player or an assistant coach.

In his first season at Nebraska (2004), Callahan finished 5–6, giving the Cornhuskers their first losing season in more than 40 years. He had introduced the West Coast offense to a program that had traditionally relied on a strong option running attack.

The Cornhuskers finished 8–4 during his second season and won the 2005 Alamo Bowl by defeating No. 20 Michigan, 32–28. The 7–4 Wolverines were the highest-ranked opponent that Nebraska had defeated since a 20–10 win over No. 2 Oklahoma in October 2001. The Wolverines also were the highest-ranked opponent defeated by Nebraska away from home since a 66–17 win over Northwestern in the 2000 Alamo Bowl.

The 2006 team finished 9–5 and won the Big 12 North for the first time since 1999. The win over then No. 24-ranked Texas A&M marked Nebraska's first ever road win over a ranked Big 12 South team.

Many expected that the 2007 season would be a breakthrough year for Nebraska. However, the team fell well short of expectations. Nebraska was beaten by USC 49–31 in a nationally televised September 15 game, being outrushed by a 313 to 31 margin but outgaining USC in the passing game 389 to 144.[9] A 41–6 thumping by Missouri started a five-game losing streak—the Huskers' first since 1958.[10] On October 15, 2007, Steve Pederson, the athletic director who had hired Callahan, was fired. Pederson was replaced on an interim basis by Nebraska's legendary former head coach, Tom Osborne.

On November 3, the Cornhuskers suffered a 76–39 pounding at the hands of Kansas. It was the most points a Cornhusker team had ever surrendered at the time. The Huskers followed this performance a week later with a win, scoring 73 points against Kansas State.

On the afternoon of November 24, 2007, a day after a 65–51 loss to rival Colorado, Callahan arrived at the team's practice facility at 6:30 a.m. He met briefly with Osborne and was fired. As he left the complex, he waved to reporters gathered outside. Osborne announced during a press conference held at the school that despite Callahan's ouster,[11] he would still earn $3.1 million as part of his buyout.[12]

While Nebraska's defense struggled during Callahan's tenure, numerous offensive school records were set (some of which could be attributed to the dramatic change in offensive philosophy) and QBZac Taylor was named Big 12 Offensive Player of the Year for 2006. Callahan's tenure as Nebraska's head coach was primarily defined by an emphasis on recruiting (something many Nebraska fans felt was lacking during the previous coach's tenure[13]). For example, with the assistance of his recruiting coordinator John Blake, Nebraska recruited DTNdamukong Suh (2009 AP Player of the Year, Nagurski Trophy winner, Heisman Trophy finalist, etc.) although Suh later stated that he would "probably be at Oregon State right now" had Callahan not been fired.[14] Callahan's 2005 recruiting class was rated as top-five by Rivals[15] and ESPN analyst Tom Lemming said they were "No. 1, without a doubt.".[16]

Despite a 27–22 record, Callahan's tenure is considered to be a failure. He led the Cornhuskers to two losing seasons in four years. He also finished ranked in a major poll only once in four years after the Huskers had only finished unranked once since 1962. He was 1–10 against teams ranked in the Top 25, 27–2 in games in which he led at halftime, 0–17 in games in which he trailed at halftime, 25–21 against Division I opponents, 15–18 against the Big 12, and coached the program to two of its four non-winning seasons in 46 years. Sports Illustrated recently[when?] named Callahan as the worst coaching hire of the decade in college football. Exacerbating Cornhusker fans' consternation with Bill Callahan's tenure at the university was his insistence that he had "done an excellent job in every area."[17]

On January 18, 2008, Callahan was hired as Assistant Head Coach of the New York Jets. On January 2, 2009 Callahan interviewed for the Head Coach of the New York Jets.

In 2008, three of the offensive linemen (with Bill Callahan as their position coach) from the Jets were named to the Pro Bowl Nick Mangold, Alan Faneca and D'Brickashaw Ferguson. All three repeated in 2009. Under Callahan's direction of the running game the Jets broke the franchise record in 2009 gaining 2756 yards on the ground through 16 regular season games. They led the National Football League in rushing and averaged 4.5-yard per attempt.

For the 2009 season, Peter King named Callahan the assistant coach of the year.[18]

Callahan was hired as the offensive line coach for the Dallas Cowboys during the 2012 off-season On June 4, 2013, owner Jerry Jones announced that Callahan would be making play calls on offense, allowing Head Coach Jason Garrett to focus on game-management.[19] After being the offensive coordinator for the Cowboys during the 2013 season, he was stripped of his play calling duties. During the 2014 off-season, Callahan was asked to interview for offensive coordinator positions with the Cleveland Browns and Baltimore Ravens but was barred from doing so. Callahan's contract as the offensive line coach expired after the 2015 season, allowing him to seek other opportunities.[20] Callahan is considered among the best offensive line coaches in the NFL and is the one behind the success of the Dallas Cowboys offensive line, having three of them (Tyron Smith, Zack Martin, and Travis Frederick) voted to the all Pro team in 2014.